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Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene

Abstract

Ever since Darwin’s pioneering research, the evolution of self-fertilisation (selfing) has been regarded as one of the most prevalent evolutionary transitions in flowering plants1,2. A major mechanism to prevent selfing is the self-incompatibility (SI) recognition system, which consists of male and female specificity genes at the S-locus and SI modifier genes2,3,4. Under conditions that favour selfing, mutations disabling the male recognition component are predicted to enjoy a relative advantage over those disabling the female component, because male mutations would increase through both pollen and seeds whereas female mutations would increase only through seeds5,6. Despite many studies on the genetic basis of loss of SI in the predominantly selfing plant Arabidopsis thaliana7,8,9,10,11,12,13,14,15, it remains unknown whether selfing arose through mutations in the female specificity gene (S-receptor kinase, SRK), male specificity gene (S-locus cysteine-rich protein, SCR; also known as S-locus protein 11, SP11) or modifier genes, and whether any of them rose to high frequency across large geographic regions. Here we report that a disruptive 213-base-pair (bp) inversion in the SCR gene (or its derivative haplotypes with deletions encompassing the entire SCR-A and a large portion of SRK-A) is found in 95% of European accessions, which contrasts with the genome-wide pattern of polymorphism in European A. thaliana16,17. Importantly, interspecific crossings using Arabidopsis halleri as a pollen donor reveal that some A. thaliana accessions, including Wei-1, retain the female SI reaction, suggesting that all female components including SRK are still functional. Moreover, when the 213-bp inversion in SCR was inverted and expressed in transgenic Wei-1 plants, the functional SCR restored the SI reaction. The inversion within SCR is the first mutation disrupting SI shown to be nearly fixed in geographically wide samples, and its prevalence is consistent with theoretical predictions regarding the evolutionary advantage of mutations in male components.

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Figure 1: The relationship between population structure and haplogroup frequencies of the S -locus and flanking genes, PUB8 and ARK3.
Figure 2: Disrupted SCR-A in A. thaliana.
Figure 3: Interspecific crosses between A. halleri and A. thaliana.
Figure 4: Restoration of functional SCR-A results in self-incompatibility and the prevention of selfing.

Accession codes

Primary accessions

GenBank/EMBL/DDBJ

Data deposits

Sequence data have been deposited to GenBank under accession numbers GU723782GU723953.

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Acknowledgements

We thank P. Awadalla, C. Bustamante, A. Caicedo, G. Coop, U. Grossniklaus, T.-h. Kao, C. Mays, R. Moore, K. Olsen, M. Purugganan, J. Reininga, L. Rose, S. Ruzsa and W. Stephan for discussions or technical advice. This work was supported by grants from the University Research Priority Program in Systems Biology/Functional Genomics of the University of Zurich and from the Swiss National Science Foundation (SNF) to K.K.S., and by Grants-in-Aid for Special Research on Priority Areas to S.T., M.W. and K.K.S.; by a grant from the Ministry of Education, Culture, Sports, Science, and Technology of Japan (MEXT) and by a Grant-in-Aid for Creative Scientific Research to S.T.; by a Young Scientific Research (S) grant to M.W.; and by a grant from the Japan Society for the Promotion of Science (JSPS). P.P. is the recipient of a grant from the Volkswagen Foundation and a STIBET scholarship of the Deutscher Akademischer Austauschdienst (DAAD). T.T. and K.S. are recipients of a Research Fellowship for Young Scientists from JSPS.

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Contributions

T.T., K.S., M.W. and K.K.S. conceived and designed the study; T.T., R.S.-I. and K.K.S. performed sequencing, genotyping and crossing experiments; T.T., P.P., T.S. and K.K.S. conducted molecular population genetic analysis; K.S., S.I., S.T. and M.W. conducted transgenic analysis; T.T., K.S., G.S., T.S., M.W. and K.K.S. wrote the paper. All authors discussed the results and commented on the manuscript.

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Correspondence to Masao Watanabe or Kentaro K. Shimizu.

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Tsuchimatsu, T., Suwabe, K., Shimizu-Inatsugi, R. et al. Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464, 1342–1346 (2010). https://doi.org/10.1038/nature08927

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